Population Ecology

, Volume 55, Issue 4, pp 585–593 | Cite as

The thermoregulatory strategy of two sympatric colubrid snakes affects their demography

  • Hervé Lelièvre
  • Philippe Rivalan
  • Virginie Delmas
  • Jean-Marie Ballouard
  • Xavier Bonnet
  • Gabriel Blouin-Demers
  • Olivier Lourdais
Original article


Population dynamics of terrestrial vertebrates are affected by climatic fluctuations, notably in ectotherms. An understanding of the interaction between physiology and demographic processes is necessary to predict the impacts of climate change. Reptiles are particularly sensitive to temperature, but only a few studies have explored the relationship between thermoregulatory strategy and demography in these animals. Using 12 years of mark-recapture data on two sympatric colubrid snakes (Hierophis viridiflavus and Zamenis longissimus), we tested whether demographic parameters are influenced by contrasted thermoregulatory strategies. The thermophilic and conspicuous species (H. viridiflavus) grew faster than the thermoconforming and secretive species (Z. longissimus), and this difference was most pronounced in open habitats, suggesting that the metabolic benefits associated with high thermal preferences depend on environmental factors at small spatial scales. Survival varied annually in both species, but was not lower in H. viridiflavus despite a higher degree of exposure. In Z. longissimus, survival was negatively affected by low temperatures during the active season, possibly underlying an exposure trade-off.


Climate Ectothermy Growth Snakes Survival Thermoregulation 


  1. Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268CrossRefGoogle Scholar
  2. Angilletta MJ, Bennett AF, Guderley H, Navas CA, Seebacher F, Wilson RS (2006) Coadaptation: a unifying principle in evolutionary thermal biology. Physiol Biochem Zool 79:282–294PubMedCrossRefGoogle Scholar
  3. Araujo MB, Thuiller W, Pearson RG (2006) Climate warming and the decline of amphibians and reptiles in Europe. J Biogeogr 33:1712–1728CrossRefGoogle Scholar
  4. Arnold SJ, Bennett AF (1984) Behavioral variation in natural populations. III. Antipredator displays in the garter snake Thamnophis radix. Anim Behav 32:1108–1138CrossRefGoogle Scholar
  5. Ayers DY, Shine R (1997) Thermal influences on foraging ability: body size, posture and cooling rate of an ambush predator, the python Morelia spilota. Funct Ecol 11:342–347CrossRefGoogle Scholar
  6. Bauwens D, Garland T Jr, Castilla AM, Van Damme R (1995) Evolution of sprint speed in Lacertid lizards: morphological, physiological and behavioral covariation. Evolution 49:848–863CrossRefGoogle Scholar
  7. Belliure J, Carrascal LM, Diaz JA (1996) Covariation of thermal biology and foraging mode in two Mediterranean Lacertid lizards. Ecology 77:1163–1173CrossRefGoogle Scholar
  8. Bennett AF (1980) The thermal dependence of lizard behavior. Anim Behav 28:752–762CrossRefGoogle Scholar
  9. Blouin-Demers G, Nadeau P (2005) The cost-benefit model of thermoregulation does not predict lizard thermoregulatory behaviour. Ecology 86:560–566CrossRefGoogle Scholar
  10. Blouin-Demers G, Prior KA, Weatherhead PJ (2002) Comparative demography of black ratsnakes (Elaphe obsoleta) in Ontario and Maryland. J Zool 256:1–10CrossRefGoogle Scholar
  11. Bonnet X, Naulleau G, Shine R (1999) The dangers of leaving home: dispersal and mortality in snakes. Biol Conserv 89:39–50CrossRefGoogle Scholar
  12. Bonnet X, Pearson DJ, Ladyman M, Lourdais O, Bradshaw SD (2002) ‘Heaven’ for serpents? A mark-recapture study of tiger snakes (Notechis scutatus) on Carnac Island, Western Australia. Austral Ecol 27:442–450CrossRefGoogle Scholar
  13. Brodie ED, Russel NH (1999) The consistency of individual differences in behaviour: temperature effects on antipredators behaviour in garter snakes. Anim Behav 57:445–451PubMedCrossRefGoogle Scholar
  14. Buckland ST, Burnham KP, Augustin NH (1997) Model selection: an integral part of inference. Biometrics 53:603–618CrossRefGoogle Scholar
  15. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. Springer, New YorkGoogle Scholar
  16. Capizzi D, Luiselli L, Capula M, Rugiero L (1995) Feeding habits of a Mediterranean community of snakes in relation to prey availability. Rev Ecol-Terre Vie 50:353–363Google Scholar
  17. Carfagno GLF, Weatherhead PJ (2008) Energetics and space use: intraspecific and interspecific comparisons of movements and home ranges of two Colubrid snakes. J Anim Ecol 77:416–424PubMedCrossRefGoogle Scholar
  18. Carrière Y, Boivin G (1997) Evolution of thermal sensitivity of parasitization capacity in egg parasitoids. Evolution 51:2028–2032CrossRefGoogle Scholar
  19. Chamaillé-Jammes S, Massot M, Aragon P, Clobert J (2006) Global warming and positive fitness response in mountain populations of common lizards Lacerta vivipara. Glob Change Biol 12:392–402CrossRefGoogle Scholar
  20. Choquet R, Lebreton JD, Gimenez O, Reboulet AM, Pradel R (2009) U-CARE: utilities for performing goodness of fit tests and manipulating capture-recapture data. Ecography 32:1071–1074CrossRefGoogle Scholar
  21. Daly BG, Dickman CR, Crowther MS (2008) Causes of habitat divergence in two species of agamid lizards in arid central Australia. Ecology 89:65–76PubMedCrossRefGoogle Scholar
  22. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672PubMedCrossRefGoogle Scholar
  23. Du WG, Shou L, Shen JY (2006) Habitat selection in two sympatric Chinese skinks, Eumeces elegans and Sphenomorphus indicus: do thermal preferences matter? Can J Zool 84:1300–1306CrossRefGoogle Scholar
  24. Dubois Y, Blouin-Demers G, Thomas DW (2008) Temperature selection in wood turtles (Glyptemys insculpta) and its implications for energetics. Écoscience 15:398–406CrossRefGoogle Scholar
  25. Garland T Jr, Adolph SC (1994) Why not to do 2-species comparative studies—Limitations on inferring adaptation. Physiol Zool 67:797–828Google Scholar
  26. Gauffre B, Estoup A, Bretagnolle V, Cosson JF (2008) Spatial genetic structure of a small rodent in a heterogeneous landscape. Mol Ecol 17:4619–4629PubMedCrossRefGoogle Scholar
  27. Gil JM, Pleguezuelos JM (2001) Prey and prey-size selection by the short-toed eagle (Circaetus gallicus) during the breeding season in Granada (south-eastern Spain). J Zool 255:131–137CrossRefGoogle Scholar
  28. Harris MP, Anker-Nilssen T, McCleery RH, Erikstad KE, Shaw DN, Grosbois V (2005) Effect of wintering area and climate on the survival of adult Atlantic puffins Fratercula arctica in the eastern Atlantic. Mar Ecol-Prog Ser 297:283–296CrossRefGoogle Scholar
  29. Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Annu Rev Physiol 67:177–201PubMedCrossRefGoogle Scholar
  30. Huey RB, Slatkin M (1976) Costs and benefits of lizard thermoregulation. Quart Rev Biol 51:363–384PubMedGoogle Scholar
  31. Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366Google Scholar
  32. Huey RB, Deutsch CA, Tewksbury JJ, Vitt LJ, Hertz PE, Perez HJA, Garland T (2009) Why tropical forest lizards are vulnerable to climate warming. Proc Roy Soc B-Biol Sci 276:1939–1948CrossRefGoogle Scholar
  33. Jaksic FM, Silva SI, Meserve PL, Gutierrez JR (1997) A long-term study of vertebrate predator responses to an El Nino (ENSO) disturbance in western South America. Oikos 78:341–354CrossRefGoogle Scholar
  34. Kearney M, Porter WP (2004) Mapping the fundamental niche: physiology, climate, and the distribution of a nocturnal lizard. Ecology 85:3119–3131CrossRefGoogle Scholar
  35. Kingsolver JG, Woods HA (1997) Thermal sensitivity of growth and feeding in Manduca sexta caterpillars. Physiol Zool 70:631–638PubMedGoogle Scholar
  36. Le Galliard JF, Marquis O, Massot M (2010) Cohort variation, climate effects and population dynamics in a short-lived lizard. J Anim Ecol 79:1296–1307PubMedCrossRefGoogle Scholar
  37. Le Galliard J-F, Massot M, Baron J-P, Clobert J (2012) Ecological effects of climate change on European reptiles. In: Brodie J, Post E, Doak D (eds) Wildlife conservation in a changing climate. University of Chicago Press, Chicago, pp 179–203Google Scholar
  38. Lelièvre H, Le Hénanff M, Blouin-Demers G, Naulleau G, Lourdais O (2010) Thermal strategies and energetics in two sympatric colubrid snakes with contrasted exposure. J Comp Physiol B 180:415–425PubMedCrossRefGoogle Scholar
  39. Lelièvre H, Blouin-Demers G, Pinaud D, Lisse H, Bonnet X, Lourdais O (2011) Contrasted thermal preferences translate into divergences in habitat use and realized performance in two sympatric snakes. J Zool 284:265–275CrossRefGoogle Scholar
  40. Lelièvre H, Legagneux P, Blouin-Demers G, Bonnet X, Lourdais O (2012) Trophic niche overlap in two syntopic colubrid snakes (Hierophis viridiflavus and Zamenis longissimus) with contrasted lifestyles. Amphibia-Reptilia 33:37–44CrossRefGoogle Scholar
  41. Lenk P, Joger U, Wink M (2001) Phylogenetic relationships among European ratsnakes of the genus Elaphe Fitzinger based on mitochondrial DNA sequence comparisons. Amphibia-Reptilia 22:329–339CrossRefGoogle Scholar
  42. Lima M, Stenseth NC, Leirs H, Jaksic FM (2003) Population dynamics of small mammals in semi-arid regions: a comparative study of demographic variability in two rodent species. Proc Roy Soc Ser B-Biol Sci 270:1997–2007CrossRefGoogle Scholar
  43. Lourdais O, Shine R, Bonnet X, Guillon M, Naulleau G (2004) Climate affects embryonic development in a viviparous snake, Vipera aspis. Oikos 104:551–560CrossRefGoogle Scholar
  44. Luiselli L (2005) Snakes don’t shrink, but ‘shrinkage’ is an almost inevitable outcome of measurement error by the experimenters. Oikos 110:199–202CrossRefGoogle Scholar
  45. Luiselli L (2006) Ecological modelling of convergence patterns between European and African ‘whip’ snakes. Acta Oecol 30:62–68CrossRefGoogle Scholar
  46. Luiselli L, Capizzi D (1997) Influences of area, isolation and habitat features on distribution of snakes in Mediterranean fragmented woodlands. Biodiv Conserv 6:1339–1351CrossRefGoogle Scholar
  47. Madsen T, Shine R (2000) Rain, fish and snakes: climatically driven population dynamics of Arafura filesnakes in tropical Australia. Oecologia 124:208–215CrossRefGoogle Scholar
  48. Marquis O, Massot M, Le Galliard JF (2008) Intergenerational effects of climate generate cohort variation in lizard reproductive performance. Ecology 89:2575–2583PubMedCrossRefGoogle Scholar
  49. McDonald PG, Olsen PD, Cockburn A (2004) Weather dictates reproductive success and survival in the Australian brown falcon Falco berigora. J Anim Ecol 73:683–692CrossRefGoogle Scholar
  50. Michel CL, Bonnet X (2010) Contrasted thermal regimes do not influence digestion and growth rates in a snake from temperate climate. Physiol Biochem Zool 83:924–931PubMedCrossRefGoogle Scholar
  51. Mondal S, Rai U (2001) In vitro effect of temperature on phagocytic and cytotoxic activities of splenic phagocytes of the wall lizard, Hemidactylus flaviviridis. Comp Biochem Physiol 129:391–398CrossRefGoogle Scholar
  52. Naulleau G (1984) Les serpents de France Revue Française d’Aquariologie, 11è année, 3 et 4, Paris (in French)Google Scholar
  53. Naulleau G (1997a) Coluber viridiflavus (Lacépède, 1789). In: Gasc JP, Cabela A, Crnobrnja-Isailovic J, Dolmen D, Grossenbacher K, Haffner P, Lescure J, Martens H, Martinez Rica JP, Maurin H, Oliveira ME, Sofianidou TS, Veith M, Zuiderwijk A (eds) Atlas of amphibians and reptiles in Europe. Societas Herpetologica et Muséum National d’Histoire Naturelle, Paris, pp 342–343Google Scholar
  54. Naulleau G (1997b) Elaphe longissima (Laurenti, 1768). In: Gasc JP, Cabela A, Crnobrnja-Isailovic J, Dolmen D, Grossenbacher K, Haffner P, Lescure J, Martens H, Martinez Rica JP, Maurin H, Oliveira ME, Sofianidou TS, Veith M, Zuiderwijk A (eds) Atlas of amphibians and reptiles in Europe. Societas Herpetologica et Muséum National d’Histoire Naturelle, Paris, pp 356–357Google Scholar
  55. Naulleau G (2003) Evolution de l’aire de répartition en France, en particulier au Centre Ouest, chez trois serpents: extension vers le nord (la Couleuvre verte et jaune, Coluber viridiflavus Lacépède et la Vipère aspic Vipera aspis Linné) et régression vers le Nord (la Vipère péliade, Vipera berus Linné). Biogeographica 79:59–69 (in French with English abstract)Google Scholar
  56. Ojanguren AF, Braña F (2000) Thermal dependence of swimming endurance in juvenile brown trout. J Fish Biol 56:1342–1347CrossRefGoogle Scholar
  57. Pike DA, Pizzatto L, Pike BA, Shine R (2008) Estimating survival rates of uncatchable animals: the myth of high juvenile mortality in reptiles. Ecology 89:607–611PubMedCrossRefGoogle Scholar
  58. Pollock KH, Nichols JD, Brownie C, Hines JE (1990) Statistical inference for capture-recapture experiments. Wildl Monogr 107:1–97Google Scholar
  59. Rugiero L, Capizzi D, Luiselli L (2002) Interactions between sympatric snakes, Coluber viridiflavus and Elaphe longissima: are there significant inter-annual differences in coexistence patterns? Ecol Mediterr 28:75–91Google Scholar
  60. Sæther BE, Tufto J, Engen S, Jerstad K, Rostad OW, Skatan JE (2000) Population dynamical consequences of climate change for a small temperate songbird. Science 287:854–856PubMedCrossRefGoogle Scholar
  61. Scheers H, Van Damme R (2002) Micro-scale differences in thermal habitat quality and a possible case of evolutionary flexibility in the thermal physiology of Lacertid lizards. Oecologia 132:323–331CrossRefGoogle Scholar
  62. Secor SM, Nagy KA (1994) Bioenergetic correlates of foraging mode for the snakes Crotalus cerastes and Masticophis flagellum. Ecology 75:1600–1614CrossRefGoogle Scholar
  63. Selas V (2001) Predation on reptiles and birds by the common buzzard, Buteo buteo, in relation to changes in its main prey, voles. Can J Zool 79:2086–2093CrossRefGoogle Scholar
  64. Shine R, Bonnet X (2009) Reproductive biology, population viability, and options for field management. In: Mullin SJ, Seigel RA (eds) Snakes: Ecology and conservation. Cornell University Press, Ithaca, pp 172–200Google Scholar
  65. Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M, Lara-Resendiz R, Martínez-Méndez N, Calderón-Espinosa ML, Meza-Lázaro RN, Gadsden H, Avila LJ, Morando M, De la Riva IJ, Sepulveda PV, Duarte Rocha CF, Ibargüengoytía N, Puntriano CA, Massot M, Lepetz V, Oksanen TA, Chapple DG, Bauer AM, Branch WR, Clobert J, Sites JW Jr (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899PubMedCrossRefGoogle Scholar
  66. Stenseth NC, Mysterud A, Ottersen G, Hurrell JW, Chan KS, Lima M (2002) Ecological effects of climate fluctuations. Science 297:1292–1296PubMedCrossRefGoogle Scholar
  67. Stevens M, Yule DH, Ruxton GD (2008) Dazzle coloration and prey movement. Proc Roy Soc B-Biol Sci 275:2639–2643CrossRefGoogle Scholar
  68. Stevenson RD, Peterson CR, Tsuji J (1985) The thermal dependence of locomotion, tongue flicking, digestion, and oxygen consumption in the wandering garter snake. Physiol Zool 58:46–57Google Scholar
  69. Weatherhead PJ, Sperry JH, Carfagno GLF, Blouin-Demers G (2012) Latitudinal variation in thermal ecology of North American ratsnakes and its implications for the effect of climate warming on snakes. J Therm Biol 37:273–281CrossRefGoogle Scholar
  70. Webb JK, Whiting MJ (2005) Why don’t small snakes bask? Juvenile broad-headed snakes trade thermal benefits for safety. Oikos 110:515–522CrossRefGoogle Scholar
  71. Webb JK, Brook BW, Shine R (2003) Does foraging mode influence life history traits? A comparative study of growth, maturation and survival of two species of sympatric snakes from south-eastern Australia. Austral Ecol 28:601–610CrossRefGoogle Scholar
  72. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–139CrossRefGoogle Scholar

Copyright information

© The Society of Population Ecology and Springer Japan 2013

Authors and Affiliations

  • Hervé Lelièvre
    • 1
    • 2
  • Philippe Rivalan
    • 1
  • Virginie Delmas
    • 1
  • Jean-Marie Ballouard
    • 1
    • 2
  • Xavier Bonnet
    • 1
  • Gabriel Blouin-Demers
    • 3
  • Olivier Lourdais
    • 1
  1. 1.Centre d’Études Biologiques de Chizé, CNRS UPR 1934Villiers en BoisFrance
  2. 2.Université de PoitiersPoitiersFrance
  3. 3.Département de biologieUniversité d’OttawaOttawaCanada

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